In 1926, the Winnipeg Art Gallery Association was formed to assist the institution in operating its museum component.

The museum moved to its present location in September 1971, with the opening of a purpose-built building designed by Gustavo da Roza.

[8] The art school, and museum operated as separate departments of the same institution, initially controlled by the bureau.

[6] The institution became independent of the bureau in April 1923, when it was formally incorporated as the Winnipeg Gallery and School of Art by the Legislative Assembly of Manitoba.

[10] The gallery resumed normal operations on 22 April 1932, when it was reopened at the Civic Auditorium's (the present Manitoba Archives Building) western wing.

"[13] In 1967, the museum acquired a triangular plot of land across from the Civic Auditorium and launched a competition for architects to submit designs for a new building.

[16] The gallery moved to its present location in 1971, into a building designed by Canadian architect Gustavo Da Roza.

[19] The Government of Nunavut collection formed in 1999, and was originally housed in the Prince of Wales Northern Heritage Centre in Yellowknife.

[21] The retail space was the result of a partnership formed between the Government of Nunavut, and the Winnipeg Art Gallery.

[22] WAG@ThePark was opened as a partnership between the Winnipeg Art Gallery and the Assiniboine Park Conservancy, which saw the museum curate exhibitions in the building.

[24] In 2018, a lost painting by Alfred Munnings was located in the permanent collections of the Winnipeg Art Gallery.

Paterson's horse, Peggy, during the First World War, and was lost shortly after a Royal Academy of Arts exhibition in 1919, which featured that piece, and 43 other works from Munnings.

[26] The lost painting was identified in the Winnipeg Art Gallery's permanent collection after a public appeal to locate the work was issued by the British National Army Museum; in their efforts to recreate the 1919 exhibition.

[15] The groundbreaking ceremony for the new building was held in May 2018, and featured the lighting of a qulliq, an Inuit drum dance, and throat singing.

[30] In 2023, the museum began the process to remove the name of former director, Ferdinand Eckhardt, from its entrance hall, after reports emerged of his Nazi-linked activities in occupied Europe.

The main building for the Winnipeg Art Gallery was opened in September 1971 and was designed by Gustavo da Roza in a late-modernist style.

[34] During the design and construction process, da Roza partnered with Number Ten Architects, who provided architectural drafting and project management.

[36] According to da Roza, the use of Tyndall stone for the load-bearing wall was selected to help affirm the "character of [the] northern prairie environment.

[15] The ground level, known as Ferdinand Eckhardt Hall, is a large space sheathed in saw-cut Tyndall stone and houses the museum's gift shop and art rental store, conservation lab, the main lobby, and a 320-seat auditorium complete this level.

[40] As of March 2015, the Winnipeg Art Gallery's permanent collection includes over 24,000 works from Canadian and international artists.

[41] Summer Afternoon, the Prairie by Lionel LeMoine FitzGerald was the first work purchased by the museum for its permanent collection.

[45] Work by Canadian artists prior to the 20th century in the museum's collection include those created by Maurice Cullen, Mary Riter Hamilton, John A. Hammond, Robert Harris, Otto Reinhold Jacobi, Paul Kane, Cornelius Krieghoff, James Wilson Morrice, Lucius Richard O'Brien, William Raphael, George Agnew Reid, Peter Rindisbacher, Frederick Arthur Verner, and Homer Watson.

[17] Other works in the collection by modern Canadian artists include Bertram Brooker, Emily Carr, Charles Comfort, Ivan Eyre, Prudence Heward, William Kurelek, David Milne, Walter J. Phillips, Tony Tascona and William H. Lobchuk and other printmakers of the Grand Western Canadian Screen Shop.

[45] The museum's also has a collection contemporary art from Canadian artists, most of which is made up equally of prints and paintings, although it also includes collages, drawings, installations, sculptures, and videos.

[45] As of March 2015, the museum's decorative art collection includes more than 4,000 works of ceramic, glass, metal, and textiles from the 17th century to the present.

[46] The museum's international art collection is made up of paintings from American and European artists from the 19th and 20th centuries.

[30] Quamajuq's inaugural exhibit was named INUA, meaning "life force" or "spirit" in some Arctic dialects.

Igloliorte comes from Nunatsiavut, Krista Ulujuk Zawadski from Nunavut, Asinnajaq from Nunavik, and Kablusiak is Inuvialuit.